A defensive symbiont and a plant virus confer direct and discrete phenotypes to a cereal aphid in a context‐dependent manner

Abstract Aphids are small sap‐feeding insects that are used as a model system for host‐endosymbiont studies. Alongside an obligate bacterial endosymbiont, aphids associate with several facultative species, while these are not essential for aphid survival they provide phenotypic benefits to host aphids. Aphids are also highly efficient vectors of many plant viruses, and association with plant viruses also influences aphid phenotype and behaviour. Thus, both endosymbionts and viruses can play important roles at the population and community level. Here, we use multiple aphid populations and virus isolates to test the interactive effects of virus presence, virus isolate and facultative endosymbionts on aphid fitness and behaviour. We focussed on a persistently transmitted virus, the primary vector of this virus, and a defensive facultative endosymbiont. We observed isolate‐dependent virus effects on winged aphid production, reproductive fitness and aphid dispersal, while endosymbionts predominantly affected aphid feeding behaviour. Endosymbiont infection led to faster initiation of plant tissue probing and increased phloem ingestion. We also identified interactions between virus isolate and endosymbiont infection on early aphid population growth rates, where the endosymbiont effect varied depending on virus isolate present. We showed that virus isolate, endosymbiont infection and combinations of these can drive differences in aphid fitness, dispersal and feeding behaviour. This work highlighted the important role of within‐species diversity for understanding aphids as vectors of important crop viruses. Future strategies for controlling pests and diseases must embrace this complexity to maximise long‐term effectiveness of management approaches.